Tumor-associated lymphocytes and increased FoxP3+ regulatory T cell frequency correlate with more aggressive papillary thyroid cancer

Journal of Clinical Endocrinology and Metabolism

Volumn 95, Issue 5, 2010, Pages 2325-2333

  French, Jena D ^a,b   Weber, Zachary J ^a   Fretwell, Deborah L ^a   Said, Sherif ^a   Klopper, Joshua P ^a,b   Haugen, Bryan R ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD20 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; THYROGLOBULIN; THYROID PEROXIDASE ANTIBODY; TRANSCRIPTION FACTOR FOXP3; TUMOR MARKER; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

ADULT; AGED; ANTIBODY BLOOD LEVEL; ARTICLE; CANCER INVASION; CANCER STAGING; CD3+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8 CD3 T LYMPHOCYTE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN TISSUE; HYPOTHESIS; IMMUNOFLUORESCENCE; IMMUNOREGULATION; LYMPH NODE METASTASIS; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RETROSPECTIVE STUDY; SOLID TUMOR; T LYMPHOCYTE SUBPOPULATION; THYROGLOBULIN BLOOD LEVEL; THYROID CANCER; THYROID FOLLICULAR CARCINOMA; THYROID INSULAR CARCINOMA; THYROID PAPILLARY CARCINOMA; THYROID TALL CELL CARCINOMA; THYROIDITIS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR VOLUME; ANTIBODY SPECIFICITY; IMMUNOLOGY; MIDDLE AGED; PAPILLARY CARCINOMA; PATHOLOGY; THYROID GLAND; THYROID TUMOR;

ADULT; AGED; AGED, 80 AND OVER; ANTIBODY SPECIFICITY; CARCINOMA, PAPILLARY; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LYMPHATIC METASTASIS; LYMPHOCYTE SUBSETS; MALE; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; RETROSPECTIVE STUDIES; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; THYROID GLAND; THYROID NEOPLASMS; YOUNG ADULT;

EID: 77952778924     PISSN: 0021972X     EISSN: 0021972X     Source Type: Journal    
DOI: 10.1210/jc.2009-2564     Document Type: Article

References (40)

1. Davies L, Welch HG 2006 Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 295:2164-2167
2. National Cancer Institute, SEER cancer statistics review 1975-2005. Bethesda, MD: National Cancer Institute
3. Lundgren CI, Hall P, Dickman PW, Zedenius J 2006 Clinically significant prognostic factors for differentiated thyroid carcinoma: a population-based, nested case-control study. Cancer 106:524-531
4. Hughes CJ, Shaha AR, Shah JP, Loree TR 1996 Impact of lymph node metastasis in differentiated carcinoma of the thyroid: a matched-pair analysis. Head Neck 18:127-132 (Pubitemid 26075352)
5. Mazzaferri EL, Jhiang SM 1994 Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med 97:418-428
6. Clark OH, Greenspan FS, Dunphy JE 1980 Hashimoto's thyroiditis and thyroid cancer: indications for operation. Am J Surg 140:65-71 (Pubitemid 10070055)
7. Hirabayashi RN, Lindsay S 1965 The relation of thyroid carcinoma and chronic thyroiditis. Surg Gynecol Obstet 121:243-252
8. Matsubayashi S, Kawai K, Matsumoto Y, Mukuta T, Morita T, Hirai K, Matsuzuka F, Kakudoh K, Kuma K, Tamai H 1995 The correlation between papillary thyroid carcinoma and lymphocytic infiltration in the thyroid gland. J Clin Endocrinol Metab 80:3421-3424
9. Gupta S, Patel A, Folstad A, Fenton C, Dinauer CA, Tuttle RM, Conran R, Francis GL 2001 Infiltration of differentiated thyroid carcinoma by proliferating lymphocytes is associated with improved disease-free survival for children and young adults. J Clin Endocrinol Metab 86:1346-1354
10. Modi J, Patel A, Terrell R, Tuttle RM, Francis GL 2003 Papillary thyroid carcinomas from young adults and children contain a mixture of lymphocytes. J Clin Endocrinol Metab 88:4418-4425
11. Zhu J, Paul WE 2008 CD4 T cells: fates, functions, and faults. Blood 112:1557-1569
12. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W 2004 Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10:942-949
13. + suppressor lymphocytes in the circulation of patients immunized against melanoma antigens. J Immunother 26:85-93
14. Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, Drebin JA, Strasberg SM, Eberlein TJ, Goedegebuure PS, Linehan DC 2002 Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 169:2756-2761
15. Wolf D, Wolf AM, Rumpold H, Fiegl H, Zeimet AG, Muller-Holzner E, Deibl M, Gastl G, Gunsilius E, Marth C 2005 The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 11:8326-8331
16. + T cells in metastatic tumor lesions from melanoma patients compared to peripheral blood. Cancer Immunol Immunother 57:1795-1805
17. Miller AM, Lundberg K, Ozenci V, Banham AH, Hellström M, Egevad L, Pisa P 2006 CD4+CD25high T cells are enriched in the tumor and peripheral blood of prostate cancer patients. J Immunol 177:7398-7405
18. Alvaro T, Lejeune M, Salvadó MT, Bosch R, García JF, Jaén J, Banham AH, Roncador G, Montalbán C, Piris MA 2005 Outcome in Hodgkin's lymphoma can be predicted from the presence of accompanying cytotoxic and regulatory T cells. Clin Cancer Res 11:1467-1473
19. Barnett B, Kryczek I, Cheng P, Zou W, Curiel TJ 2005 Regulatory T cells in ovarian cancer: biology and therapeutic potential. Am J Reprod Immunol 54:369-377
20. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, Harris AL, Banham AH 2006 Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 24:5373-5380
21. Carreras J, Lopez-Guillermo A, Fox BC, Colomo L, Martinez A, Roncador G, Montserrat E, Campo E, Banham AH 2006 High numbers of tumor-infiltrating FOXP3-positive regulatory T cells are associated with improved overall survival in follicular lymphoma. Blood 108:2957-2964
22. Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, Biota C, Doffin AC, Durand I, Olive D, Perez S, Pasqual N, Faure C, Ray-Coquard I, Puisieux A, Caux C, Blay JY, Ménétrier-Caux C 2009 Regulatory T cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res 69:2000-2009
23. Bluestone JA, Abbas AK 2003 Natural versus adaptive regulatory T cells. Nat Rev Immunol 3:253-257
24. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J Exp Med 198:1875-1886
25. Vigouroux S, Yvon E, Biagi E, Brenner MK 2004 Antigen-induced regulatory T cells. Blood 104:26-33
26. Zhou G, Levitsky HI 2007 Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumor-specific tolerance. J Immunol 178:2155-2162
27. Dannull J, Su Z, Rizzieri D, Yang BK, Coleman D, Yancey D, Zhang A, Dahm P, Chao N, Gilboa E, Vieweg J 2005 Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells. J Clin Invest 115:3623-3633
28. Saenger YM, Wolchok JD 2008 The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases. Cancer Immun 8:1
29. American Joint Committee on Cancer 2002 AJCC cancer staging handbook: TNM classification of malignant tumors. 6th ed. New York: Springer-Verlag
30. Soh EY, Duh QY, Sobhi SA, Young DM, Epstein HD, Wong MG, Garcia YK, Min YD, Grossman RF, Siperstein AE, Clark OH 1997 Vascular endothelial growth factor expression is higher in differentiated thyroid cancer than in normal or benign thyroid. J Clin Endocrinol Metab 82:3741-3747
31. Vasko V, Espinosa AV, Scouten W, He H, Auer H, Liyanarachchi S, Larin A, Savchenko V, Francis GL, de la Chapelle A, Saji M, Ringel MD 2007 Gene expression and functional evidence of epithelial-tomesenchymal transition in papillary thyroid carcinoma invasion. Proc Natl Acad Sci USA 104:2803-2808
32. Gabrilovich D 2004 Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat Rev Immunol 4:941-952 (Pubitemid 39620069)
33. Cao X 2009 Regulatory T cells and immune tolerance to tumors. Immunol Res 10.1007/s12026-009-8124-7
34. Kaminska B, Wesolowska A, Danilkiewicz M 2005 TGFβ signalling and its role in tumour pathogenesis. Acta Biochim Pol 52:329-337
35. Russell JP, Engiles JB, Rothstein JL 2004 Proinflammatory mediators and genetic background in oncogene mediated tumor progression. J Immunol 172:4059-4067
36. Ryder M, Ghossein RA, Ricarte-Filho JC, Knauf JA, Fagin JA 2008 Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocr Relat Cancer 15:1069-1074
37. Ugolini C, Basolo F, Proietti A, Vitti P, Elisei R, Miccoli P, Toniolo A 2007 Lymphocyte and immature dendritic cell infiltrates in differentiated, poorly differentiated, and undifferentiated thyroid carcinoma. Thyroid 17:389-393
38. Sfanos KS, Bruno TC, Maris CH, Xu L, Thoburn CJ, DeMarzo AM, Meeker AK, Isaacs WB, Drake CG 2008 Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin Cancer Res 14:3254-3261
39. + regulatory T cells in the peripheral blood of patients with prostate cancer. Clin Cancer Res 14:1032-1040
40. Mansfield AS, Heikkila PS, Vaara AT, von Smitten KA, Vakkila JM, Leidenius MH 2009 Simultaneous Foxp3 and IDO expression is associated with sentinel lymph node metastases in breast cancer. BMC Cancer 9:231